Epigenetic reprogramming rewires transcription during the alternation of generations in Arabidopsis
Abstract
Alternation between morphologically distinct haploid and diploid life forms is a defining feature of most plant and algal life cycles, yet the underlying molecular mechanisms that govern these transitions remain unclear. Here, we explore the dynamic relationship between chromatin accessibility and epigenetic modifications during life form transitions in Arabidopsis. The diploid-to-haploid life form transition is governed by the loss of H3K9me2 and DNA demethylation of transposon-associated cis-regulatory elements. This event is associated with dramatic changes in chromatin accessibility and transcriptional reprogramming. In contrast, the global loss of H3K27me3 in the haploid form shapes a chromatin accessibility landscape that is poised to re-initiate the transition back to diploid life after fertilization. Hence, distinct epigenetic reprogramming events rewire transcription through major reorganization of the regulatory epigenome to guide the alternation of generations in flowering plants.
Data availability
Deep-sequencing data that support the findings of this study have been deposited in the Gene Expression Omnibus (GEO) under accession code GSE155369. Re-analysis of previously published DNA methylomes from dme-2/+ pollen (Ibarra et al., 2012), and siRNAs from leaves (Papareddy et al., 2020) and pollen (Borges et al., 2018; Slotkin et al., 2009) were deposited in the GEO under accession code GSE155369.
-
Epigenetic reprogramming rewires transcription during the alternation of generations in ArabidopsisNCBI Gene Expression Omnibus, GSE155369.
-
Active DNA demethylation in plant companion cells reinforces transposon methylation in gametesNCBI Gene Expression Omnibus, GSE38935.
-
Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatinNCBI Gene Expression Omnibus, GSE120669.
-
Transposon-derived small RNAs triggered by miR845 mediate genome dosage response in ArabidopsisNCBI Gene Expression Omnibus, GSE106117.
-
Epigenetic reprogramming and small RNA silencing of transposable elements in pollenNCBI Gene Expression Omnibus, GSE61028.
Article and author information
Author details
Funding
Austrian Science Fund (P26887)
- Frédéric Berger
Austrian Science Fund (I 4258)
- Frédéric Berger
Austrian Science Fund (I2163-B16)
- Frédéric Berger
Austrian Science Fund (M1818)
- Michael Borg
European Commission (ERC 637888)
- Michael D Nodine
Biotechnology and Biological Sciences Research Council (BB/I011269/1)
- David Twell
Biotechnology and Biological Sciences Research Council (BB/N005090)
- David Twell
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2021, Borg et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 6,111
- views
-
- 895
- downloads
-
- 67
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Developmental Biology
Rhythmic and sequential segmentation of the growing vertebrate body relies on the segmentation clock, a multi-cellular oscillating genetic network. The clock is visible as tissue-level kinematic waves of gene expression that travel through the presomitic mesoderm (PSM) and arrest at the position of each forming segment. Here, we test how this hallmark wave pattern is driven by culturing single maturing PSM cells. We compare their cell-autonomous oscillatory and arrest dynamics to those we observe in the embryo at cellular resolution, finding similarity in the relative slowing of oscillations and arrest in concert with differentiation. This shows that cell-extrinsic signals are not required by the cells to instruct the developmental program underlying the wave pattern. We show that a cell-autonomous timing activity initiates during cell exit from the tailbud, then runs down in the anterior-ward cell flow in the PSM, thereby using elapsed time to provide positional information to the clock. Exogenous FGF lengthens the duration of the cell-intrinsic timer, indicating extrinsic factors in the embryo may regulate the segmentation clock via the timer. In sum, our work suggests that a noisy cell-autonomous, intrinsic timer drives the slowing and arrest of oscillations underlying the wave pattern, while extrinsic factors in the embryo tune this timer’s duration and precision. This is a new insight into the balance of cell-intrinsic and -extrinsic mechanisms driving tissue patterning in development.
-
- Developmental Biology
- Neuroscience
The blood-brain barrier (BBB) controls the movement of molecules into and out of the central nervous system (CNS). Since a functional BBB forms by mouse embryonic day E15.5, we reasoned that gene cohorts expressed in CNS endothelial cells (EC) at E13.5 contribute to BBB formation. In contrast, adult gene signatures reflect BBB maintenance mechanisms. Supporting this hypothesis, transcriptomic analysis revealed distinct cohorts of EC genes involved in BBB formation and maintenance. Here, we demonstrate that epigenetic regulator’s histone deacetylase 2 (HDAC2) and polycomb repressive complex 2 (PRC2) control EC gene expression for BBB development and prevent Wnt/β-catenin (Wnt) target genes from being expressed in adult CNS ECs. Low Wnt activity during development modifies BBB genes epigenetically for the formation of functional BBB. As a Class-I HDAC inhibitor induces adult CNS ECs to regain Wnt activity and BBB genetic signatures that support BBB formation, our results inform strategies to promote BBB repair.